The Hippocampus Generalizes across Memories that Share Item and Context Information

Libby, Laura A.; Reagh, Zachariah M.; Bouffard, Nichole R; Ragland, J. Daniel; Ranganath, Charan

doi:10.1162/jocn_a_01345

Cited by 32 publications

(27 citation statements)

References 57 publications

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“…Accordingly, we maintain that both source memory and pattern separation rely on complex hippocampal circuits rather than distinct regions. Indeed, a recent study by Libby et al (2018) found that patterns of hippocampal activity discriminated among similar items and similar contexts, but generalized across similar items-in-context, suggesting complex interactions. However, the dissociated signals elicited by source memory and pattern separation in the present study indicate that these processes may rely on distinct neural mechanisms that can be identified when the two processes are pitted against each other in an experimental design.…”

Section: Discussionmentioning

confidence: 99%

Pattern Separation and Source Memory Engage Distinct Hippocampal and Neocortical Regions during Retrieval

et al. 2019

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Detailed representations of past events rely on the ability to form associations between items and their contextual features (i.e., source memory), as well as the ability to distinctly represent a new event from a similar one stored in memory (i.e., pattern separation). These processes are both known to engage the hippocampus, although whether they share similar mechanisms remains unclear. It is also unknown if, and in which region(s), activity related to these processes overlaps and/or interacts. Here, we used high-resolution fMRI to examine the contributions of hippocampal subfields and neocortical areas to pattern separation and source memory with an experimental paradigm that concurrently tested both. During encoding, male and female human subjects incidentally studied items in one of four quadrants on the screen. During test, they viewed repeated items (targets), similar items (lures), and new items (foils) and were asked to indicate whether each item was old, similar, or new. Following each item judgment, subjects were asked to indicate the quadrant in which the original stimulus was presented. Thus, each lure trial had a lure discrimination component (taxing pattern separation) and a location judgment (source memory). We found two main response profiles: (1) pattern separation-related signals in DG/CA3 and perirhinal cortex and (2) source memory signals in posterior CA1, parahippocampal cortex, and angular gyrus. Whole-brain voxelwise analysis revealed that activity related to lure discrimination and source memory was largely nonoverlapping. These findings suggest that distinct processes underlie the retrieval of pattern separated item representations and recollection of source information.

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Section: Discussionmentioning

confidence: 99%

Pattern Separation and Source Memory Engage Distinct Hippocampal and Neocortical Regions during Retrieval

et al. 2019

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“…Beta images went through a second visual inspection to make sure all the deviant trials were excluded. This noise trial exclusion procedure is adopted from the previous pattern similarity studies in the lab (Libby, Reagh, Bouffard, Ragland, & Ranganath, 2019).…”

Section: Pattern Similarity Analysismentioning

confidence: 99%

Representation of Task Structure in Human Hippocampus and Orbitofrontal Cortex

Mızrak

Bouffard

Libby

et al. 2019

Preprint

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Memories of previous experiences can be used to guide future decisions in similar situations. Recent evidence suggests that the hippocampus might support decision-making by forming representations that capture common elements across different events (e.g., "cognitive maps" or "schemas"). Here, we used functional magnetic resonance imaging (fMRI) to test how the human hippocampus represents decision relevant information extracted from previous experiences. Participants performed a task in which they learned to predict a customer preference for foods in four different store contexts. The task was structured such that we could examine the degree to which hippocampal representations reflected generalized information about the store contexts, food items, and also the kind of information that was relevant to decisions on a given trial. Results showed that hippocampal activity patterns carried information about the kind of information that was currently relevant to a decision. Across different store contexts, hippocampal representations differentiated between context-determined (deterministic) decisions and context-invariant (probabilistic) decisions. Results also showed that information about store contexts was represented by the hippocampus, but contrary to what might be expected, similar contexts were hyperdifferentiated from one another. These results suggest that the hippocampus may support decision-making by systematically mapping relationships between task relevant information, decisions, and outcomes.

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“…Context-dependent memory with neutral valence -in contrast to contextual classical or operant conditioning [8]-is in humans often experimentally investigated via the combined presentation of items -like faces [9][10][11][12], everyday objects [11][12][13][14], or words [15,16]-and contexts -like scene pictures [9][10][11][12]15,16], words [14] or sounds [13]-in a computer task [17].…”

Section: Introductionmentioning

confidence: 99%

“…In rodents, the most widely used task to assess neutral context-dependent memory uses physical objects instead of virtual items. This task is commonly known as the object-incontext task (OIC) [18] and relies on the hippocampal system and associated cortical regions [1,19], comparable to human context-dependent memory [14,17,20]. In the OIC test the hippocampal system is needed to establish the link between the object's features and the contextual features; that is, without the hippocampal system an animal is able to remember the object in the sense of familiarity, but not remember the context in which it was encountered [19].…”

Section: Introductionmentioning

confidence: 99%

“… Time of learning trials between 7.5 -minutes 14  Testing in last learning context  minutes learning trials 26  Counterbalanced testing in first and last learning context 27 All in all, the current study illustrates that insights from historical datasets can help to interpret data from control animals, which can next be used to increase power of future studies [64]. Performing an unbiased data-driven analysis of metadata may form the basis for more consensus on the set-up, procedure and interpretation of the OIC task for rodents; and hence for recommendations how to design future studies.…”

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Measuring context-dependent memory in rodents: a systematic review and meta-analysis of important variables in the object-in-context task

Sep

Vellinga

Sarabdjitsingh

et al. 2021

Preprint

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Environmental information plays an important role in remembering events. Information about stable aspects of the environment (here referred to as ‘context’) and the event are combined by the hippocampal system and stored as context-dependent memory. In rodents (such as rats and mice), context-dependent memory is often investigated with the object-in-context task. However, the implementation and interpretation of this task varies considerably across studies. This variation hampers the comparison between studies and - for those who design a new experiment or carry out pilot experiments – the estimation of whether observed behavior is within the expected range. Also, it is currently unclear which of the variables critically influence the outcome of the task. To address these issues, we carried out a preregistered systematic review (PROSPERO CRD42020191340) and provide an up-to-date overview of the animal-, task-, and protocol-related variations in the object-in-context task for rodents. Using a data-driven explorative meta-analysis we next identified critical factors influencing the outcome of this task, such as sex, testbox size and the delay between the learning trials. Based on these observations we provide recommendations to create more consensus in the set-up, procedure and interpretation of the object-in-context task for rodents. This could contribute to a more robust and evidence-based design in future animal experiments.

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The Hippocampus Generalizes across Memories that Share Item and Context Information

Cited by 32 publications

References 57 publications

Pattern Separation and Source Memory Engage Distinct Hippocampal and Neocortical Regions during Retrieval

Pattern Separation and Source Memory Engage Distinct Hippocampal and Neocortical Regions during Retrieval

Representation of Task Structure in Human Hippocampus and Orbitofrontal Cortex

Measuring context-dependent memory in rodents: a systematic review and meta-analysis of important variables in the object-in-context task

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